Nasopulmonary mites (Halarachnidae) of coastal Californian pinnipeds: Identity, prevalence, and molecular characterization

Abstract

Mites from the family Halarachnidae Oudemans 1906 are obligate endoparasites that colonize the respiratory tracts of free-living and captive marine mammals. Infestations can range from mild to severe and result in respiratory tract irritation or impairment. Nasopulmonary acariasis was determined to be a contributing cause of death among several southern sea otters Enhydra lutris nereis Merriam 1904 in a longitudinal study of otter mortality, and proximity to Pacific harbor seals Phoca vitulina richardii Gray 1864 was a significant risk factor for sea otter infestation. Beyond scattered opportunistic reports, each halarachnid mite species' affinity for particular hosts and the extent of mite transmission between host species is poorly understood. We investigated the identity and prevalence of nasopulmonary mites from Pacific harbor seals, California sea lions Zalophus californianus Lesson 1828, northern elephant seals Mirounga angustirostris Gill 1866, northern fur seals Callorhinus ursinus Linnaeus 1758, and Guadalupe fur seals Arctocephalus philippii townsendi Merriam 1897 to complement published nasopulmonary mite findings from sympatric southern sea otters during a comparable timeframe. Halarachnid mite infestation was common among California sea lions (74.1%), northern fur seals (73.3%), and northern elephant seals (46.6%), but was less common among harbor seals (18.7%) and Guadalupe fur seals (8.8%). Observed host-mite relationships suggest a distinct host specificity, with genus Orthohalarachne infesting otariids, and genus Halarachne infesting phocids and lutrinids along the California coast. Harbor seals and southern sea otters were the primary hosts of H. halichoeri , but one nothern elephant seal was infested with both H. miroungae and a single H. halichoeri. We also present the first high-resolution SEM images for H. miroungae and O. attenuata and possible evidence for a new host record for H. halichoeri .

First report of a severe nasopulmonary acariasis caused by Orthohalarachne diminuata Doetschman, 1944 (Acari: Halarachnidae) in a captive South American sea lion (Otaria flavescens Shaw, 1800)

“…Mesostigmatid mites of the genera Halarachne Allman, 1847 and Orthohalarachne Newell, 1947 belonging to the family Halarachnidae Oudemans, 1906 constitute obligatory endoparasites infesting the respiratory tract of different semiaquatic marine mammals. Thereby, representatives of the genus Halarachne parasitize pinnipeds of the family Phocidae Gray, 1821 (earless seals) and sea otters ( Enhydra lutris Linnaeus, 1758), while the genus Orthohalarachne occurs in pinnipeds of the order Otariidae Gray, 1825 (eared seals) and Odobenidae Allen, 1880 (walruses) ( Kim et al, 1980 ; Rolbiecki et al, 2018 ; Seguel et al, 2018a ; Reckendorf et al, 2019 ; Pesapane et al, 2021 ). Within the genus Orthohalarachne , two species (with various synonyms) have been described: O. attenuata Banks, 1910 infesting nasopharyngeal mucosa, and O. diminuata Doetschman, 1944 parasitizing in parts of the upper and the lower respiratory tract ( Kim et al, 1980 ; Rolbiecki et al, 2018 ).…”

Nasopulmonary mites (Acari: Halarachnidae) as potential vectors of bacterial pathogens, including Streptococcus phocae, in marine mammals

“…Notably, many mite species demonstrate relatively low host specificity. Halarachne halichoeri infestations have been reported in eight marine host species [ 15 , 119 , 120 ] and Orthohalarachne attenuata in fourteen marine host species [ 15 , 119 ], suggesting broad exchange of halarachnid mites among proximate marine mammal populations [ 2 , 13 , 120 ]. As a result, NPM could mechanically or biologically vector bacteria and other pathogens within and between mammalian host species.…”

“…phocae and other bacterial pathogens of marine mammals. Given that NPMs are globally distributed and relatively abundant across marine mammal populations [ 12 , 16 , 119 , 120 ], including imperiled species like the southern sea otter and the Guadalupe fur seal ( Arctocephalus philippii townsendi ) [ 2 , 15 ], the potential for transmission of opportunistic bacterial pathogens is concerning. This potential for pathogen spread between animals should be considered for animal translocation programs, and co-housing of animals in rehabilitation facilities, zoos, aquaria, and oil spill response settings.…”

“…Collectively our findings contribute to an improved understanding of the host-parasite microbial community which can inform veterinary treatment, captive animal care, and animal conservation and translocation efforts. Prior captive care is a risk factor for NPM infestation in wild sea otter populations [ 13 ], and NPM parasitism can be very high in captivity without regular acaricidal treatment [ 1 , 4 , 121 ], and NPM are found in marine mammals worldwide [ 15 , 119 , 120 ]. As a result, our work has important implications for preventing pathogen transmission during captive care, oil spill response, and animal reintroduction efforts globally.…”

“…lutris nereis ) morbidity and mortality, with up to one quarter of fresh dead otters necropsied between 2012 and 2017 harboring NPM [ 2 , 13 , 14 ]. In a complementary study of sympatric pinnipeds, the prevalence of NPM infestation ranged from 8.8% to 74.1% among pinniped populations [ 15 ]. The piercing mouthparts of NPMs damage surface epithelium while consuming bodily fluids [ 9 ] resulting in mucosal irritation, respiratory illness, and secondary infection [ 1 , 10 – 13 , 16 ].…”